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COMMENTARY
The speciation revolution
J. MALLET
Galton Laboratory, University College London, London, UK
I predict the years 1990±2010 will be seen as a revolution
in the study of speciation. One person's punctuated
equilibrium is another's gradual change, and the current
revolution is in any case paltry compared with Darwin's
own. Even so, many previously accepted beliefs about
speciation are now doubted, and features of a classic
scienti®c revolution are evident.
To see just how much has changed, consider what
experts were saying until recently. Coyne (1994), for
example, listed four major achievements due to Ernst
Mayr since the 1940s. These were: (1) an appreciation of
the reality of species (as compared with, say, the
unreality of subspecies or genera); (2) the reproductive
isolation de®nition of species (the `biological species
concept'); (3) the generality of allopatric speciation; and
(4) founder-effect speciation. Coyne (1994) argued that
Mayr's fourth achievement, the founder effect, was
probably incorrect, but regarded the other three as
completely in tune with the current view of speciation.
What is extraordinary about this list is that all these
`achievements' are now, only 7 years later, rejected by
major groups of evolutionary biologists. Softening on
points (1) and (4) are found today even in papers coauthored by Coyne himself (Kliman et al., 2000; Turelli
et al., 2001). The opinions under attack date from the
1930s to the 1950s, and are identi®ed strongly with
Theodosius Dobzhansky and Ernst Mayr; however, virtually all evolutionary biologists and most textbooks
supported these ideas until the late 1980s. In what
follows, I discuss each of Coyne's points in turn.
1 Reality of species is now doubted by many. Coyne
(1994) argued that Mayr was one of the ®rst to recognize
that discontinuities between species were real. Personally, I ®nd this hard to support, as discontinuities are
what everyone uses to distinguish species, and always
did: `species ¼ do not at any one period present an
inextricable chaos of varying and intermediate links'
(Darwin, 1859, p. 177). The Dobzhansky/Mayr innovation was the idea that species were more discontinuous or
`real' than either higher or lower taxa. Today, an
essentialist species `reality' strongly con¯icts with our
understanding of gradual speciation, and is no longer
1 accepted at all generally (Bachmann, 1998; Kliman et al.,
Correspondence: James Mallet, Galton Laboratory, University College
London, 4 Stephenson Way, London NW1 2HE, UK.
Tel.: +44-171-380-7412/7411; fax: +44-171-383-2048;
e-mail: [email protected]
J. EVOL. BIOL. 14 (2001) 887±888 ã 2001 BLACKWELL SCIENCE LTD
2000; Mallet, 2001). Wu (2001) makes the same point in
this issue: speciation is a process of emerging genealogical
distinctness, rather than a discontinuity affecting all
genes simultaneously.
2 Reproductive isolation is no longer generally recognized
as the best de®nition of species. One does not need to
take sides to realize that we are in an intense period of
navel-gazing about what species are, and therefore what
speciation itself is. Some have argued that the confusion
is caused by unruly scientists each promoting their own,
hair-splittingly different species concept. But there is, I
believe, more to it than that. Real con¯icts exist, driven
by real new data, particularly from ecological and
molecular studies of natural populations. All this philosophizing is a classic symptom of scienti®c revolutions: `it
is, I think, particularly in times of acknowledged crisis
[i.e. during scienti®c revolutions] that scientists have
turned to philosophical analysis as a device for unlocking
the riddles of their ®eld' (Kuhn, 1970, p. 88).
Wu (2001) provides a good example of the revolutionary process. Wu's many papers follow in the tradition
of Drosophila speciation work begun by Dobzhansky, but
he now pauses to challenge a central dogma of his school,
the reproductive isolation concept. Wu (2001) is no
anarchist. Instead, he ®nds total reproductive isolation
meaningless given evidence for transfer of genes between
closely related Drosophila species. Other loci within the
same genomes become genealogically distinct, either
because they contribute directly to selection against
hybrids, or because they are trapped in parts of the
genome contributing to such selection (Wang et al.,
1997; Wu, 2001).
3 Speciation does not require allopatry. The idea that
speciation can occur only in allopatry had been accepted
generally since the 1940s (Coyne, 1994), whereas the
idea that parapatric and sympatric speciation are also
probable is completely acceptable today (Gavrilets et al.,
2000; Jiggins & Mallet, 2000; Turelli et al., 2001; Via,
2001).
4 Natural selection is becoming viewed as the primary
cause of speciation. Dobzhansky and Mayr argued that
allopatry, in conjunction with founder events and ecological selection, caused speciation. In the 1970s, it was
pointed out that divergent natural selection might
outweigh gene ¯ow even at very small spatial scales
(Bush, 1975; Endler, 1977). This in turn led to the
proposal that natural selection was a primary cause of
speciation, rather than allopatry (Barton & Charlesworth,
1984; Schilthuizen, 2000). At ®rst, this argument became
entangled in a debate about reinforcement (Butlin,
1989), but it is increasingly evident that selection can
also reduce assortative mating more simply, as a
by-product of divergent adaptation. Adaptive divergence
887
888
J. MALLET
can cause reduced gene ¯ow, which in turn allows
further divergence, and so on, until speciation is
2 achieved (e.g. Dieckmann & Doebeli, 1999; Via, 2001).
Is it really a revolution? Some might view these
U-turns as mere improvements, but at the very least
changes are speeding up. For instance, it took about
10 years after the discovery that host races of Rhagoletis
were genetically differentiated (Feder et al., 1988) before
nonallopatric adaptation and speciation was seen as
likely in other systems. Today the pace is accelerating:
arguments for ecological speciation and sympatric and/or
parapatric differentiation are ¯ooding in (Jiggins &
Mallet, 2000; Schluter, 2001; Via, 2001).
An extraordinary feature of the current revolution is
the strength of rapprochement with Darwin's own views.
This has been noted independently several times (e.g.
Mallet, 1995; Schilthuizen, 2000; Kondrashov, 2001).
Today's rejection of the reality of species was foreshadowed by Darwin ± `we shall have to treat species in the
same manner as ¼ naturalists treat genera¼' (Darwin,
1859, p. 484), as was a de-emphasis of reproductive
isolation ± `I do not think that the very general fertility of
varieties can be proved to be of universal occurrence, or
to form a fundamental distinction between varieties and
species' (Darwin, 1859, p. 271). Darwin recognized the
existence of allopatric speciation, of course, but argued
that competition in large diverse ecosystems was more
important: `Although I do not doubt that [geographical]
isolation is of considerable importance in the production
of new species, on the whole I am inclined to believe that
largeness of area is of more importance' (Darwin, 1859,
p. 105). Finally, Darwin believed that selection and
competition caused speciation, long before Mayr's now
discredited founder event model of speciation was presented. I know of no other scienti®c revolution that
involves such a renaissance of the paradigm-before-last.
We are apparently emerging from a 60-year-old blind
alley, a veritable Dark Ages compared with the typical
pace of modern science. During this time, important data
was of course being accumulated, fostered by these very
ideas of Dobzhansky and Mayr that we now question, so
the time was not wasted. As an end result, we do now
seem to be achieving what the `modern synthesis' of the
1930s and 1940s ®rst attempted: a fusion of Darwinism
and genetics into a general theory of speciation.
Note: I have kept references to a minimum at the
behest of the editor. I have therefore omitted citations,
especially to Dobzhansky and Mayr's many works (references are readily available in other articles in this
issue), and to the many recent examples showing how
ecological adaptation may commonly lead to assortative
mating as a by-product (1995±2001).
References
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J. EVOL. BIOL. 14 (2001) 887±888 ã 2001 BLACKWELL SCIENCE LTD